Marine Biology

, Volume 161, Issue 1, pp 111–118 | Cite as

Latitude or biogeographic breaks? Determinants of phenotypic (co)variation in fitness-related traits in Betaeus truncatus along the Chilean coast

  • Aura M. Barria
  • Marco A. Lardies
  • Andrew P. Beckerman
  • Leonardo D. Bacigalupe
Original Paper


Ectothermal organisms distributed along environmental gradients in a wide geographical distribution display extensive phenotypic variation. This is particularly pervasive along latitudinal clines, which are linked to gradual changes in environmental factors. Widespread species may also be distributed among biogeographic breaks, which in contrast to smooth clines, often show abrupt changes in phenotypic traits. In species with widespread latitudinal distribution that also encompass important biogeographical breaks, it is not clear which of those factors prevails on shaping the phenotypic variation or if some traits are particularly more sensitive to one or the other. To evaluate this, we measured 4 fitness-related traits in 6 populations of the intertidal snapping shrimp Betaeus truncatus, as its distribution along Chile expands over 40° in latitude and three major biogeographical provinces. Here, we statistically evaluated the role of both, latitude and biogeographic breaks, on mean population values of fitness-related traits but also on the variances and covariances (i.e., P-matrix) between them. Overall, our results (1) indicate that latitude is more important than breaks in shaping the phenotypic variation of most of these fitness-related traits, (2) show that the differences in the variance–covariance relationship among traits between the extremes of the gradient arises from gradual increases in variance and rather sharp changes in covariance at mid-latitudes and (3) show that at present, it is difficult to unambiguously determine whether natural selection or plasticity is responsible for the observed pattern in means, variances and covariances and only further work might disentangle these possibilities.



Aura M. Barria acknowledges a CONICYT Doctoral Fellowship. This research was funded by FONDECYT 1110743 to Marco A. Lardies, by CONICYT MEC 800120004 to Andrew P. Beckerman and by FONDECYT 1120461 to Leonardo D. Bacigalupe. This study complies with current Chilean legislation regarding the collection and treatment of invertebrates.


  1. Albornoz L, Wehrtmann IS (1997) Descripción y clave de los primeros estadíos larvales de camarones carídeos (Decapoda: Hippolytidae, Alpheidae, Rhynchocinetidae) de aguas costeras de Chile. Invest Mar Valparaíso 25:121–133Google Scholar
  2. Arntz W, Gorny M (1996) Cruise report of the Chilean–German–Italian Magellan “Victor Hensen” Campaign in 1994. Ber Polarforsch 190:1–113Google Scholar
  3. Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H, Moreteau B (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18:700–706CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B (2013). lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2.
  5. Bauer RT (1992) Testing generalization about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebr Reprod Dev 22:193–202CrossRefGoogle Scholar
  6. Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36(2):216–236Google Scholar
  7. Brante A, Fernández M, Viard F (2012) Phylogeography and biogeography concordance in the marine gastropod Crepipatella dilatata (Calyptraeidae) along the southern eastern pacific coast. J Hered. doi: 10.1093/jhered/ess030 Google Scholar
  8. Camus PA (2001) Biogeografía marina de Chile continental. Rev Chil Hist Nat 74:587–617CrossRefGoogle Scholar
  9. Cardenas L, Castilla JC, Viard F (2009) A phylogeographic analysis across three biogeographic provinces of the southeastern Pacific: the case of the marine gastropod Concholepas concholepas. J Biogeogr 36:969–981CrossRefGoogle Scholar
  10. Clarke A (1987) Temperature, latitude and reproductive output. Mar Biol 38:89–99Google Scholar
  11. Clarke A (1992) Reproduction in the cold: Thorson revisited. Invertebr Reprod Dev 22:175–184CrossRefGoogle Scholar
  12. Clarke A, Hopkins CCE, Nilssen EM (1991) Egg size and reproductive output in the deepwater prawn Pandalus borealis Krøyer, 1838. Funct Ecol 5:724–730CrossRefGoogle Scholar
  13. Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients. Ann NY Acad Sci 1168:100–129CrossRefGoogle Scholar
  14. Cowen RK, Paris CB, Srinivasan A (2006) Scaling connectivity in marine populations. Science 311:522–527CrossRefGoogle Scholar
  15. Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369CrossRefGoogle Scholar
  16. Hamilton AM, Klein ER, Austin CC (2010) Biogeographic breaks in Vanuatu, a nascent oceanic archipelago. Pac Sci 64:149–159CrossRefGoogle Scholar
  17. Haye PA, Varela AI, Thiel M (2012) Genetic signatures of rafting dispersal in algal-dwelling brooders Limnoria spp. (Isopoda) along the SE Pacific (Chile). Mar Ecol Prog Ser 455:111–122CrossRefGoogle Scholar
  18. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485CrossRefGoogle Scholar
  19. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309CrossRefGoogle Scholar
  20. Kingsolver JG, Izem R, Ragland GJ (2004) Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves. Integr Comp Biol 44:450–460CrossRefGoogle Scholar
  21. Krzanowski WJ (1979) Between-group comparisons of principal components. J Am Stat Assoc 74:703–707Google Scholar
  22. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 36:1210–1226CrossRefGoogle Scholar
  23. Lardies MA, Castilla JC (2001) Latitudinal variation in the reproductive biology of commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar Biol 139:1125–1133CrossRefGoogle Scholar
  24. Lardies MA, Wehrtmann IS (1997) Egg production in Betaeus emarginatus (H. Milne Edwards, 1837) (Decapoda: Alpheidae): fecundity, reproductive output and chemical composition of eggs. Ophelia 49:165–174CrossRefGoogle Scholar
  25. Lardies MA, Wehrtmann IS (2001) Latitudinal variation in the reproductive biology of Betaeus truncatus (Decapoda: Alpheidae) along the Chilean coast. Ophelia 55:55–67CrossRefGoogle Scholar
  26. Lardies MA, Medina M, Correa J (2008) Breakage of intraspecific patterns in coastal zones associated with copper mine tailings in Chile: the snapping shrimp Betaeus emarginatus as model. Mar Ecol Prog Ser 358:203–210CrossRefGoogle Scholar
  27. Lardies MA, Arias MB, Bacigalupe LD (2010) Phenotypic covariance matrix in life-history traits along a latitudinal gradient: a study case in a geographically widespread crab on the coast of Chile. Mar Ecol Prog Ser 412:179–187CrossRefGoogle Scholar
  28. Lardies MA, Muñoz JL, Paschke KA, Bozinovic F (2011) Latitudinal variation in the aerial/aquatic ratio of oxygen consumption of a supratidal high rocky-shore crab. Mar Ecol 32:42–51CrossRefGoogle Scholar
  29. Macaya EC, Zuccarello GC (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112CrossRefGoogle Scholar
  30. Meneses I, Santelices B (2000) Patterns and breaking points in the distribution of benthic algae along the temperate Pacific coast of South America. Rev Chil Hist Nat 73:615–623CrossRefGoogle Scholar
  31. Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8:845–856CrossRefGoogle Scholar
  32. Mizera F, Meszéna G (2003) Spatial niche packing, character displacement and adaptive speciation along an environmental gradient. Evol Ecol Res 5:363–382Google Scholar
  33. Ovaskainen O, Cano JM, Merilä J (2008) A Bayesian framework for comparative quantitative genetics. Proc R Soc Lond B 275:669–678CrossRefGoogle Scholar
  34. Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am Zool 31(1):65–80Google Scholar
  35. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna AustriaGoogle Scholar
  36. Ragionieri L, Fratini S, Vannini M, Schubart CD (2009) Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Mol Phylogenet Evol 52(3):825–834CrossRefGoogle Scholar
  37. Ricklefs RE, Wikelski M (2002) The physiology/life history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  38. Rivadeneira MM, Fernandez M, Navarrete SA (2002) Latitudinal trends of species diversity in rocky intertidal herbivore assemblages: spatial-scale and the relationship between local and regional species richness. Mar Ecol Prog Ser 245:123–131CrossRefGoogle Scholar
  39. Robinson MR, Beckerman AP (2013) Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history. Ecol Lett 16(3):281–290CrossRefGoogle Scholar
  40. Roff DA, Prokkola JM, Krams I, Rantala MJ (2012) There is more than one way to skin a G matrix. J Evol Biol 25(6):1113–1126CrossRefGoogle Scholar
  41. Sanchez R, Sepulveda RD, Brante A, Cardenas L (2011) Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Mar Ecol Prog Ser 434:121–131CrossRefGoogle Scholar
  42. Sanford E, Kelly KW (2011) Local adaptation in marine invertebrates. Ann Rev Mar Sci 3:509–535CrossRefGoogle Scholar
  43. Sanford E, Roth MS, Johns GC, Wares JP, Somero GN (2003) Local selection and latitudinal variation in a marine predator–prey interaction. Science 300:1135–1137CrossRefGoogle Scholar
  44. Silva N, Rojas N, Fedele A (2009) Water masses in the Humboldt Current System: properties, distribution, and the nitrate deficit as a chemical water mass tracer for equatorial subsurface water off Chile. Deep Sea Res Part II 56:1004–1020CrossRefGoogle Scholar
  45. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  46. Takahashi Y, Morita S, Yoshimura J, Watanabe M (2011) A geographic cline induced by negative frequency-dependent selection. BMC Evol Biol 11:256CrossRefGoogle Scholar
  47. Tellier F, Meynard AP, Correa JA, Faugeron S, Valero M (2009) Phylogeographic analyses of the 30°S south–east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: vicariance or parapatry? Mol Phylogenet Evol 53:679–693CrossRefGoogle Scholar
  48. Thiel M, Macaya E, Acuña E, Arntz W et al (2007) The Humboldt Current System of northern and central Chile: oceanographic processes, ecological interactions and socioeconomic feedback. Oceanogr Mar Biol Annu Rev 45:195–344Google Scholar
  49. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45CrossRefGoogle Scholar
  50. Waters JM (2008) Driven by the west wind drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. J Biogeogr 35(3):417–427CrossRefGoogle Scholar
  51. Wehrtmann IS, Carvacho A (1997) New records and distribution ranges of shrimps (Crusta cea: Decapoda: Penaeoidea and Caridea) in Chilean waters. Proc Biol Soc Wash 110:49–57Google Scholar
  52. West BT, Welch KB, Gałecki AT, Gillespie BW (2007) Linear mixed models: a practical guide using statistical software. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  53. Zakas C, Binford J, Navarette SA, Wares JP (2009) Upwelling-driven community transitions reflected in limited barnacle gene flow. Mar Ecol Prog Ser 394:165–177CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Aura M. Barria
    • 1
  • Marco A. Lardies
    • 2
  • Andrew P. Beckerman
    • 3
    • 1
  • Leonardo D. Bacigalupe
    • 1
  1. 1.Instituto de Ciencias Ambientales y Evolutivas, Facultad de CienciasUniversidad Austral de ChileValdiviaChile
  2. 2.Departamento de Ciencias, Facultad de Artes Liberales and Facultad de Ingeniería y CienciasUniversidad Adolfo IbañezSantiagoChile
  3. 3.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

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